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The Genus Leccinum (Boletaceae, Boletales) from China Based on Morphological and Molecular Data

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The Genus Leccinum (Boletaceae, Boletales) from China Based on Morphological and Molecular Data Journal of Fungi Article The Genus Leccinum (Boletaceae, Boletales) from China Based on Morphological and Molecular Data Xin Meng 1,2,3, Geng-Shen Wang 1,2,3, Gang Wu 1,2, Pan-Meng Wang 1,2,3, Zhu L. Yang 1,2,* and Yan-Chun Li 1,2,* 1 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; [email protected] (X.M.); [email protected] (G.-S.W.); [email protected] (G.W.); [email protected] (P.-M.W.) 2 Yunnan Key Laboratory for Fungal Diversity and Green Development, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China 3 College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, China * Correspondence: [email protected] (Z.L.Y.); [email protected] (Y.-C.L.) Abstract: Leccinum is one of the most important groups of boletes. Most species in this genus are ectomycorrhizal symbionts of various plants, and some of them are well-known edible mushrooms, making it an exceptionally important group ecologically and economically. The scientific problems related to this genus include that the identification of species in this genus from China need to be verified, especially those referring to European or North American species, and knowledge of the phylogeny and diversity of the species from China is limited. In this study, we conducted multi- locus (nrLSU, tef1-a, rpb2) and single-locus (ITS) phylogenetic investigations and morphological observisions of Leccinum from China, Europe and North America. Nine Leccinum species from China, including three new species, namely L. album, L. parascabrum and L. pseudoborneense, were revealed Citation: Meng, X.; Wang, G.-S.; Wu, and described. Leccinum album is morphologically characterized by the white basidioma, the white G.; Wang, P.-M.; Yang, Z.L.; Li, Y.-C. hymenophore staining indistinct greenish blue when injured, and the white context not changing The Genus Leccinum (Boletaceae, color in pileus but staining distinct greenish blue in the base of the stipe when injured. Leccinum Boletales) from China Based on parascabrum is characterized by the initially reddish brown to chestnut-brown and then pale brownish Morphological and Molecular Data. J. Fungi 2021, 7, 732. https://doi.org/ to brown pileus, the white to pallid and then light brown hymenophore lacking color change when 10.3390/jof7090732 injured, and the white context lacking color change in pileus but staining greenish blue in the base of the stipe when injured. Leccinum pseudoborneense is characterized by the pale brown to dark brown Academic Editors: Anush Kosakyan, pileus, the initially white and then brown hymenophore lacking color change when injured, and Rodica Catana and Alona Biketova the white context in pileus and stipe lacking color change in pileus but staining blue in stipe when bruised. Color photos of fresh basidiomata, line drawings of microscopic features and detailed Received: 28 May 2021 descriptions of the new species are presented. Accepted: 31 August 2021 Published: 6 September 2021 Keywords: boletes; taxonomy; morphology; phylogeny; new taxa Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. The genus Leccinum Gray is a species-rich genus of Boletaceae and is characterized by a whitish or yellow hymenophore, a white to cream context unchanging or staining blue or red when injured, a brown to blackish scabrous to dotted squamules on the surface of the stipe, and comparatively long and smooth basidiospores. Generally, most species Copyright: © 2021 by the authors. of the genus are widely spread in the subarctic, boreal, temperate and Mediterranean Licensee MDPI, Basel, Switzerland. regions, with a few secondary expansions to the neotropics [1–12]. Species in Leccinum This article is an open access article are both ecologically and economically important. Most species of this genus exhibit distributed under the terms and conditions of the Creative Commons mycorrhizal host specificity. Species of Leccinum sect. Scabra Smith & Thiers are associated Attribution (CC BY) license (https:// with plants of Betula, while species of L. sect. Fumosa (A.H. Smith, Thiers & Watling) Gelardi creativecommons.org/licenses/by/ are associated with plants of Populus. In L. sect. Leccinum, species are found exclusively 4.0/). associated with plants of Populus (e.g., L. albostipitatum den Bakker & Noordel. and L. insigne J. Fungi 2021, 7, 732. https://doi.org/10.3390/jof7090732 https://www.mdpi.com/journal/jof J. Fungi 2021, 7, 732 2 of 18 A.H. Sm., Thiers & Watling), Betula (e.g., L. atrostipitatum A.H. Sm., Thiers & Watling), Pinaceae (e.g., L. vulpinum Watling and L. piceinum Pilát & Dermek) and Ericaceae that form arbutoidmycorrhizas (e.g., L. manzanitae Thiers and L. monticola Halling & G.M. Muell.). However, there are species in section Leccinum that are not host specific, i.e., L. aurantiacum (Bull.) Gray. This species is associated with plants of Betula, Populus, Quercus, Salix and sometimes with Tilia [13,14]. Some species of this genus are well-known edible mushrooms, such as L. quercinum (Pilát) E.E. Green & Watling, L. scabrum (Bull.) Gray and L. versipelle (Fr. & Hök) Snell, which are collected in China during the mushroom season. The genus Leccinum was established by Gray in 1821 [13], based on the type species L. aurantiacum. Subsequently, more and more mycologists noticed the morphological distinctness and described many new species of this genus. As currently circumscribed, the genus comprises roughly 150 species [1–3,6–56]. North America is the species diversity center of this genus, and in total 118 species have been recorded from this area [19]. Some of the most important works are the serial works of Smith and Thiers [1,15–17], in which three sections of this genus were proposed (L. sect. Leccinum Smith & Thiers, L. sect. Luteoscabra Smith & Thiers and L. sect. Scabra), with 68 species described from Michigan. Twelve species from Central America were described: one species from Belize, eight species from Costa Rica and three species from Colombia [20–24]. In Europe, Singer divided species of this genus into four sections, including two known sections, L. sect. Luteoscabra and L. sect. Leccinum, and two newly proposed sections, L. sect. Roseoscabra and L. sect. Eximia [3]. In Singer’s infrageneric classification, L. sect. Scabra, established by Smith and Thiers, was merged to L. sect. Leccinum. Recent molecular phylogenetic evidence has revealed that species of L. sect. Luteoscabra, L. sect. Roseoscabra and L. sect. Eximia belong to divergent clades of Boletaceae and represent many new genera (32,52–54). Thus, the genus Leccinum is restricted to the section Leccinum (Singer’s infrageneric classification) [3]. den Bakker and Noordelos revised the European Leccinum species based on morphology and nrLSU sequences and documented sixteen species [14]. In their subsequent study, they treated the three subclades revealed by den Bakker et al. in L. section Leccinum [33,57] as three subsections (viz. L. subsect. Leccinum, L. subsect. Fumosa A.H. Sm., Thiers & Watling and L. subsect. Scabra Pilat & Dermek) [14]. This infrageneric subdivision was followed in the treatment of the genus in this study. In the Southern Hemisphere, four species have been reported, including one from New Zealand and three from Australia [27–29]. In Asia, six species of Leccinum have been reported from Malaysia [6]; ten species from Japan [7–10]; and a total of 31 species have been reported from China based on an extensive literature review [34–36,38–52,56]. Among these Chinese species, twelve species, viz. L. albellum (Peck) Singer, L. chromapes (Frost) Singer, L. crocipodium (Letell.) Watling, L. eximium (Peck) Singer, L. extremiorientale (Lar. N. Vassiljeva) Singer, L. griseum (Quél.) Singer, L. hortonii (A.H. Sm. & Thiers) Hongo & Nagas., L. nigrescens (Richon & Roze) Singer, L. rubropunctum (Peck) Singer, L. rubrum M. Zang, L. rugosiceps (Peck) Singer and L. subglabripes (Peck) Singer have been transferred to other genera [5,11,35,52–55]; eight species, viz. L. duriusculum (Schulzer ex Fr.) Singer, L. intusrubens (Corner) Høil., L. oxydabile (Singer) Singer, L. quercinum, L. rufum (Schaeff.) Kreisel, L. subleucophaeum E.A. Dick & Snell, L. subradicatum Hongo and L. variicolor Watling were reported without specimen support [39–43,49,51]; and eleven species, viz. L. ambiguum A.H. Sm. & Thiers, L. atrostipitatum A.H. Sm., Thiers & Watling, L. aurantiacum, L. holopus (Rostk.) Watling, L. olivaceopallidum A.H. Sm., Thiers & Watling, L. potteri A.H. Sm., Thiers & Watling, L. roseofractum Watling, L. scabrum, L. subgranulosum A.H. Sm. & Thiers, L. subleucophaeum var. minimum C.S. Bi and L. versipelle were reported with specimen citations [34,38,44–48]. Among these eleven species reported with specimen citations, only L. subleucophaeum var. minimum was originally described from China, and the remaining species were identified as species originally described from Europe and North America based on general morphological similarities. Indeed, a few species described from Europe and North America do occur in China, especially in northeastern and northwestern China. However, J. Fungi 2021, 7, 732 3 of 18 most species found in China have evolved independently in the southern part of China. Thus, identification of the Chinese Leccinum species needs to be reconfirmed. In this study, we used both morphological data and molecular sequences from the nu- clear ribosomal internal transcribed spacer (ITS), the large subunit of the nuclear ribosomal RNA (nrLSU), the translation elongation factor 1-alpha (tef1-a) and the RNA polymerase II second largest subunit (rpb2), together with ecological data to (1) elucidate species diversity of Leccinum in China; (2) evaluate the phylogenetic relationships of species within Leccinum; (3) make morphological and ecological comparisons between closely related species. 2. Materials and Methods 2.1.
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